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Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows

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Abstract

This study presents the first application of metabolomics to evaluate changes in rumen metabolites of dairy cows fed increasing proportions of barley grain (i.e., 0, 15, 30, and 45% of diet dry matter). 1H-NMR spectroscopy was used to analyze rumen fluid samples representing 4 different diets. Results showed that for cows fed 30 and 45% grain, increases were observed in the concentration of rumen methylamine as well as glucose, alanine, maltose, propionate, uracil, valerate, xanthine, ethanol, and phenylacetate. These studies also revealed lower rumen 3-phenylpropionate in cows fed greater amounts of cereal grain. Furthermore, ANOVA tests showed noteworthy increases in rumen concentrations of N-nitrosodimethylamine, dimethylamine, lysine, leucine, phenylacetylglycine, nicotinate, glycerol, fumarate, butyrate, and valine with an enriched grain diet. Using principal component analysis it was also found that each of the 4 diets could be distinguished on the basis of the measured rumen metabolites. The two closest clusters corresponded to the 0 and 15% grain diets, whereas the 45% barley grain diet was significantly separated from the other clusters. Unhealthly levels of a number of potentially toxic metabolites were found in the rumen of cattle fed 30 and 45% grain diets. These results may have a number of implications regarding the influence of grain on the overall health of dairy cows.

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References

  • Allison, M. J., Dougherty, R. W., Bucklin, J. A., & Snyder, E. E. (1964). Ethanol accumulation in the rumen after overfeeding with readily fermentable carbohydrate. Science, 144, 54–55.

    Article  CAS  PubMed  Google Scholar 

  • Ametaj, B. N., Bradford, B. J., Bobe, G., Nafikov, R. A., Lu, Y., Young, J. W., et al. (2005). Strong relationships between mediators of the acute phase response and fatty liver in dairy cows. Canadian Journal of Animal Science, 85, 165–175.

    Google Scholar 

  • Andries, J. I., Buysse, F. X., Debrabander, D. L., & Cottyn, B. G. (1987). Isoacids in ruminant nutrition: their role in ruminal and intermediary metabolism and possible influences on performances—a review. Animal Feed Science and Technology, 18, 169–180.

    Article  CAS  Google Scholar 

  • Bertram, H. C., Kristensen, N. B., Malmendal, A., Nielsen, N. C., Brod, R., Andersen, H. J., et al. (2005). A metabolomic investigation of splanchnic metabolism using 1H NMR spectroscopy of bovine blood plasma. Analytica Chimica Acta, 536, 1–6.

    Article  CAS  Google Scholar 

  • Bertram, H. C., Kristensen, N. B., Vestergaard, M., Jensen, S. K., Sehested, J., Nielsen, N. C., et al. (2009). Metabolic characterization of rumen epithelial tissue from dairy calves fed different starter diets using 1H NMR spectroscopy. Livestock Science, 120, 127–134.

    Article  Google Scholar 

  • Boudonck, K. J., Mitchell, M. W., Wulff, J., & Ryals, J. A. (2010). Characterization of the biochemical variability of bovine milk using metabolomics. Metabolomics. doi:10.1007/s11306-009-0160-8.

    Google Scholar 

  • Broadhurst, D. I., & Kell, D. B. (2006). Statistical strategies for avoiding false discoveries in metabolomics and related experiments. Metabolomics, 2, 171–196.

    Article  CAS  Google Scholar 

  • Bugaut, M. (1987). Occurrence, absorption and metabolism of short chain fatty acids in the digestive tract of mammals. Comparative Biochemistry and Physiology, 86B, 439–472.

    CAS  Google Scholar 

  • Burlingame, R., & Chapman, P. J. (1983). Catabolism of phenylpropionic acid and its 3-hydroxy derivative by Escherichia coli. Journal of Bacteriology, 155, 113–121.

    CAS  PubMed  Google Scholar 

  • Canadian Council on Animal Care. (1993). Guide to the care and use of experimental animals (2nd ed., Vol. 1). Ottawa: CCAC.

    Google Scholar 

  • Chesson, A., Provan, G. J., Russell, W. R., Scobbie, L., Richardson, A. J., & Stewart, C. (1999). Hydroxycinnamic acids in the digestive tract of livestock and humans. Journal of the Science of Food and Agriculture, 79, 373–378.

    Article  CAS  Google Scholar 

  • Davis, E. J., & De Ropp, R. S. (1961). Metabolic origin of urinary methylamine in the rat. Nature, 190, 636–637.

    Article  CAS  PubMed  Google Scholar 

  • Dieterle, F., Ross, A., Schlotterbeck, G., & Senn, H. (2006). Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Analytical Chemistry, 78, 4281–4290.

    Article  CAS  PubMed  Google Scholar 

  • Dumas, M.-E., Barton, R. H., Toye, A., Cloarec, O., Blancher, Ch., Rothwell, A., et al. (2006). Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proceedings of National Academy of Sciences USA, 103, 12511–12516.

    Article  CAS  Google Scholar 

  • Emmanuel, D. G. V., Dunn, S. M., & Ametaj, B. N. (2008). Feeding high proportions of barley grain stimulates an inflammatory response in dairy cows. Journal of Dairy Science, 91, 606–614.

    Article  CAS  PubMed  Google Scholar 

  • Enomoto, N., Ikejima, K., Yamashina, S., Hirose, M., Shimizu, H., Kitamura, T., et al. (2001). Kupffer cell sensitization by alcohol involves increased permeability to gut-derived endotoxin. Alcoholism, Clinical and Experimental Research, 25, 51S–54S.

    Article  CAS  PubMed  Google Scholar 

  • Estruch, R., Nicolás, J. M., Villegas, E., Jonqué, A., & Urbano-Márquez, A. (1993). Relationship between ethanol-related diseases and nutritional status in chronically alcoholic men. Alcohol and Alcoholism, 28, 543–550.

    CAS  PubMed  Google Scholar 

  • Gould, G. W. (1970). Germination and the problem of dormancy. Journal of Applied Bacteriology, 33, 34–49.

    CAS  PubMed  Google Scholar 

  • Hashimoto, S., Kawai, Y., & Mutai, M. (1975). In vitro N-nitrosodimethylamine formation by some bacteria. Infection and Immunity, 11, 1405–1406.

    CAS  PubMed  Google Scholar 

  • Hill, K. J., & Mangan, J. L. (1964). The formation and distribution of methylamine in the ruminant digestive tract. Biochemistry Journal, 93, 39–45.

    CAS  Google Scholar 

  • Hoogenraad, N. J., & Hird, F. J. R. (1970). The chemical composition of rumen bacteria and cell walls from rumen bacteria. British Journal of Nutrition, 24, 119–127.

    Article  CAS  PubMed  Google Scholar 

  • Iqbal, S., Zebeli, Q., Mazzolari, A., Bertoni, G., Dunn, S. M., et al. (2009). Feeding barley grain steeped in lactic acid modulates rumen fermentation patterns and increases milk fat content in dairy cows. Journal of Dairy Science, 92, 6023–6032.

    Article  CAS  PubMed  Google Scholar 

  • Jenkins, T. C., & McGuire, M. A. (2006). Major advances in nutrition: impact on milk composition. Journal of Dairy Science, 89, 1302–1310.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, K. A., & Johnson, D. E. (1995). Methane emissions from cattle. Journal of Animal Science, 73, 2483–2492.

    CAS  PubMed  Google Scholar 

  • Khafipour, E., Li, S., Plaizier, J. C., & Krause, D. O. (2009). Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Applied and Environmental Microbiology, 75, 7115–7124.

    Article  CAS  PubMed  Google Scholar 

  • Koppang, N. (1964). An outbreak of toxic liver injury in ruminants. Nord Veterinaermed, 16, 305–322.

    Google Scholar 

  • Kristensen, N. B., Storm, A., Raun, B. M., Røjen, B. A., & Harmon, D. L. (2007). Metabolism of silage alcohols in lactating dairy cows. Journal of Dairy Science, 90, 1364–1377.

    Article  CAS  PubMed  Google Scholar 

  • Lijinsky, W. (1999). N-Nitroso compounds in the diet. Mutation Research, 443, 129–138.

    CAS  PubMed  Google Scholar 

  • Littell, R. C., Henry, P. R., & Ammerman, C. B. (1998). Statistical analysis of repeated measures data using SAS procedures. Journal of Animal Science, 76, 1216–1231.

    CAS  PubMed  Google Scholar 

  • Martin, A. K. (1982). The origin of urinary aromatic compounds excreted by ruminants 3. The metabolism of phenolic compounds to simple phenols. British Journal of Nutrition, 48, 497–507.

    Article  CAS  PubMed  Google Scholar 

  • McAllan, A. B., & Smith, R. H. (1973). Degradation of nucleic acids in the rumen. British Journal of Nutrition, 29, 331–345.

    Article  CAS  PubMed  Google Scholar 

  • Neill, A. R., Grime, D. W., & Dawson, R. M. (1978). Conversion of choline methyl groups through trimethylamine into methane in the rumen. Biochemistry Journal, 170, 529–535.

    CAS  Google Scholar 

  • Nocek, J. E. (1997). Bovine acidosis: implications on laminitis. Journal Dairy Science, 80, 1005–1028.

    Article  CAS  Google Scholar 

  • NRC. (2001). Nutrient requirements of dairy cattle (7th rev. edn). National Academy of Sciences, Washington, DC.

  • Örlygsson, J., Anderson, R., & Svensson, B. H. (1995). Alanine as an end product during fermentation of monosaccharides by Clostridium strain P2. Antonie van Leeuwenhoek, 68, 273–280.

    Article  PubMed  Google Scholar 

  • Pagella, J. H. (1998). Urinary benzylated compounds as potential markers of forage intake and metabolism of their precursors in ruminants. PhD Dissertation, Aberdeen University, UK.

  • Pruett, B. S., & Pruett, S. B. (2006). An explanation for the paradoxical induction and suppression of an acute phase response by ethanol. Alcohol, 39, 105–110.

    Article  CAS  PubMed  Google Scholar 

  • Rieu-Lesme, F., Dauga, C., Morvan, B., Bouvet, O. M. M., Grimont, P. A. D., & Doré, J. (1996). Acetogenic sporulating cocci isolated from the rumen. Research in Microbiology, 147, 753–764.

    Article  CAS  PubMed  Google Scholar 

  • Satter, L. D., & Esdale, W. J. (1968). In vitro lactate metabolism by ruminal ingesta. Applied Microbiology, 16, 680–688.

    CAS  PubMed  Google Scholar 

  • Saude, E. J., Slupsky, C. M., & Sykes, B. D. (2006). Optimization of NMR analysis of biological fluids for quantitative accuracy. Metabolomics, 2, 113–123.

    Article  CAS  Google Scholar 

  • Seo, J. (2005). Information visualization design for multidimensional data: integrating the rank-by-feature framework with hierarchical clustering. Ph.D. Dissertation, University of Maryland.

  • Slyter, L. L. (1976). Influence of acidosis on rumen function. Journal of Animal Science, 43, 910–929.

    CAS  PubMed  Google Scholar 

  • Souliotis, V. L., Henneman, J. R., Reed, C. D., Chhabra, S. K., Diwan, B. A., Anderson, L. M., et al. (2002). DNA adducts and liver DNA replication in rats during chronic exposure to N-nitrosodimethylamine (NDMA) and their relationships to the dose-dependence of NDMA hepatocarcinogenesis. Mutation Research, 500, 75–87.

    CAS  PubMed  Google Scholar 

  • Tajima, K., Arai, S., Ogata, K., Nagamine, T., Matsui, H., Nakamura, M., et al. (2000). Rumen bacterial community transition during adaptation to high-grain diet. Anaerobe, 6, 273–284.

    Article  CAS  Google Scholar 

  • Trent, M. S., Stead, C. M., Tran, A. X., & Hankins, J. V. (2006). Diversity of endotoxin and its impact on pathogenesis. Journal of Endotoxin Research, 12, 205–223.

    Article  CAS  PubMed  Google Scholar 

  • Turlin, E., Perrotte, M., Danchin, A., & Biville, F. (2001). Regulation of the early steps of 3-phenylpropionate catabolism in Escherichia coli. Journal of Molecular Microbiology and Biotechnology, 3, 127–133.

    CAS  PubMed  Google Scholar 

  • Turlin, E., Sismeiro, O., Le Caer, J. P., Labas, V., Danchin, A., & Biville, F. (2005). 3-phenylpropionate catabolism and the Escherichia coli oxidative stress response. Research in Microbiology, 156, 312–321.

    Article  CAS  PubMed  Google Scholar 

  • Vinayavekhin, N., Homan, E. A., & Saghatelian, A. (2010). Exploring disease through metabolomics. American Chemical Society Chemical Biology, 5, 91–103.

    CAS  PubMed  Google Scholar 

  • Weljie, A. M., Newton, J., Mercier, P., Carlson, E., & Slupsky, C. M. (2006). Targeted profiling: Quantitative analysis of 1H NMR metabolomics data. Analytical Chemistry, 78, 4430–4442.

    Article  CAS  PubMed  Google Scholar 

  • Wishart, D. S. (2008a). Metabolomics: Applications to food science and nutrition research. Trends in Food Science and Technology, 19, 482–493.

    Article  CAS  Google Scholar 

  • Wishart, D. S. (2008b). Quantitative metabolomics using NMR. Trends in Analytical Chemistry, 27, 228–237.

    Article  CAS  Google Scholar 

  • Wishart, D. S., Lewis, M. J., Morrissey, J. A., Flegel, M. D., Jeroncic, K., Xiong, Y., et al. (2008). The human cerebrospinal fluid metabolome. Journal of Chromatography B, Analytical Technologies in the Biomedical and Life Sciences, 871, 164–173.

    Article  CAS  PubMed  Google Scholar 

  • Xia, J., Psychogios, N., Young, N. & Wishart, D. S. (2009). MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Research, 37(Web Server issue), W652–W660.

    Google Scholar 

  • Yu, P., Xin, H., Lu, L., Fan, H., Kazachkov, M., Jiang, Z. J., et al. (2006). Involvement of semicarbazide-sensitive amine oxidase-mediated deamination in lipopolysaccharide-induced pulmonary inflammation. American Journal of Pathology, 168, 718–726.

    Article  CAS  PubMed  Google Scholar 

  • Zebeli, Q., & Ametaj, B. N. (2009). Relationships between rumen lipopolysaccharide and mediators of inflammatory response with milk fat production and efficiency in dairy cows. Journal of Dairy Science, 92, 3800–3809.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We acknowledge co-leading of the project entitled ‘Profiling of Dairy Cattle Metabolome’ by Drs. Ametaj and Wishart, which was supported financially by the Alberta Agricultural Research Institute (AARI; Edmonton, Alberta, Canada), the Alberta Livestock Industry Development Fund (ALIDF; Edmonton, Alberta, Canada), and the Natural Sciences and Engineering Research Council of Canada (NSERC; Ottawa, Ontario, Canada). The technical assistance of D. G. V. Emmanuel, R. P. Pandian, and S. Sivaraman (University of Alberta, Edmonton, Alberta, Canada) is highly appreciated. We also are grateful to the technical staff of Dairy Research and Technology Centre at the University of Alberta for their help and care to the cows used in this study.

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Correspondence to Burim N. Ametaj.

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Ametaj, B.N., Zebeli, Q., Saleem, F. et al. Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows. Metabolomics 6, 583–594 (2010). https://doi.org/10.1007/s11306-010-0227-6

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